Gene and protein expression profile of naive and osteo-chondrogenically differentiated rat bone marrow-derived mesenchymal progenitor cells

International Journal of Molecular Medicine

Volumn 23, Issue 6, 2009, Pages 745-755

  Grässel, Susanne ^a   Ahmed, Nazish ^b   Göttl, Claudia ^a   Grifka, Joachim ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b MOUNT SINAI HOSPITAL   (Canada)

Author keywords

Chondrogenic; Mesenchymal progenitor cells; Osteogenic; Profiling; Rat

Indexed keywords

COLLAGEN TYPE 2; COLLAGEN TYPE 2A1; COLLAGENASE 3; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT 2; GELATINASE A; MONOCYTE CHEMOTACTIC PROTEIN 1; NUCLEAR RECEPTOR NUR77; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX4; TRANSCRIPTION FACTOR SOX6; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VASCULOTROPIN A;

ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; BONE MARROW CELL; CELL CULTURE; CELL DIFFERENTIATION; CHONDROGENESIS; CONTROLLED STUDY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; IN VITRO STUDY; MALE; MESENCHYMAL STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT; STEM CELL;

ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELLS, CULTURED; CHEMOKINE CCL2; CHEMOKINES, CXC; CHONDROGENESIS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; MESENCHYMAL STEM CELLS; NERVE GROWTH FACTOR; OSTEOGENESIS; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TISSUE INHIBITOR OF METALLOPROTEINASE-1; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 67649565425     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm_00000188     Document Type: Article

References (66)

1. Cancedda R, Dozin B, Giannoni P and Quarto R: Tissue engineering and cell therapy of cartilage and bone. Matrix Biol 22: 81-91, 2003.
2. Friedenstein AJ, Gorskaja JF and Kulagina NN: Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 4: 267-274, 1976.
3. Bruder SP, Fink DJ and Caplan AI: Mesenchymal stem cells in bone development, bone repair, and skeletal regeneration therapy. J Cell Biochem 56: 283-294, 1994.
4. Quarto R, Mastrogiacomo M, Cancedda R, Kutepov SM, Mukhachev V, Lavroukov A, Kon E and Marcacci M: Repair of large bone defects with the use of autologous bone marrow stromal cells. N Engl J Med 344: 385-386, 2001.
5. Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WW, Gordon PL, Neel M, Sussman M, Orchard P, Marx JC, Pyeritz RE and Brenner MK: Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 5: 309-313, 1999.
6. Mao JJ: Stem-cell-driven regeneration of synovial joints. Biol Cell 97: 289-301, 2005.
7. Raghunath J, Salacinski HJ, Sales KM, Butler PE and Seifalian AM: Advancing cartilage tissue engineering: the application of stem cell technology. Curr Opin Biotechnol 16: 503-509, 2005.
8. Wakitani S, Imoto K, Yamamoto T, Saito M, Murata N and Yoneda M: Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees. Osteoarthritis Cartilage 10: 199-206, 2002.
9. Litzke LE, Wagner E, Baumgaertner W, Hetzel U, Josimovic-Alasevic O and Libera J: Repair of extensive articular cartilage defects in horses by autologous chondrocyte transplantation. Ann Biomed Eng 32: 57-69, 2004.
10. Wilke MM, Nydam DV and Nixon AJ: Enhanced early chondrogenesis in articular defects following arthroscopic mesenchymal stem cell implantation in an equine model. J Orthop Res 25: 913-925, 2007.
11. Wagner W, Wein F, Seckinger A, Frankhauser M, Wirkner U, Krause U, Blake J, Schwager C, Eckstein V, Ansorge W and Ho AD: Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 33: 1402-1416, 2005.
12. Gerstenfeld LC, Cullinane DM, Barnes GL, Graves DT and Einhorn TA: Fracture healing as a post-natal developmental process: molecular, spatial, and temporal aspects of its regulation. J Cell Biochem 88: 873-884, 2003.
13. Tsuchida H, Hashimoto J, Crawford E, Manske P and Lou J: Engineered allogeneic mesenchymal stem cells repair femoral segmental defect in rats. J Orthop Res 21: 44-53, 2003.
14. Gysin R, Wergedal JE, Sheng MH, Kasukawa Y, Miyakoshi N, Chen ST, Peng H, Lau KH, Mohan S and Baylink DJ: Ex vivo gene therapy with stromal cells transduced with a retroviral vector containing the BMP4 gene completely heals critical size calvarial defect in rats. Gene Ther 9: 991-999, 2002.
15. Yamazaki M, Nakajima F, Ogasawara A, Moriya H, Majeska RJ, and Einhorn TA: Spatial and temporal distribution of CD44 and osteopontin in fracture callus. J Bone Joint Surg Br 81: 508-515, 1999.
16. Asahina I, Sampath TK, Nishimura I and Hauschka PV: Human osteogenic protein-1 induces both chondroblastic and osteoblastic differentiation of osteoprogenitor cells derived from newborn rat calvaria. J Cell Biol 123: 921-933, 1993.
17. Jackson RA, McDonald MM, Nurcombe V, Little DG and Cool SM: The use of heparan sulfate to augment fracture repair in a rat fracture model. J Orthop Res 24: 636-644, 2006.
18. Li J, Ahmad T, Bergstrom J, Samnegard E, Erlandsson-Harris H, Ahmed M and Kreicbergs A: Differential bone turnover in an angulated fracture model in the rat. Calcif Tissue Int 75: 50-59, 2004.
19. Yanada S, Ochi M, Adachi N, Nobuto H, Agung M and Kawamata S: Effects of CD44 antibody- or RGDS peptide-immobilized magnetic beads on cell proliferation and chondrogenesis of mesenchymal stem cells. J Biomed Mater Res A 77: 773-784, 2006.
20. Bruder SP, Jaiswal N, Ricalton NS, Mosca JD, Kraus KH and Kadiyala S: Mesenchymal stem cells in osteobiology and applied bone regeneration. Clin Orthop Relat Res 355: S247-S256, 1998.
21. Ju YJ, Muneta T, Yoshimura H, Koga H and Sekiya I: Synovial mesenchymal stem cells accelerate early remodeling of tendon-bone healing. Cell Tissue Res 332: 469-478, 2008.
22. Hadjiargyrou M, Lombardo F, Zhao S, Ahrens W, Joo J, Ahn H, Jurman M, White DW and Rubin CT: Transcriptional profiling of bone regeneration. Insight into the molecular complexity of wound repair. J Biol Chem 277: 30177-30182, 2002.
23. Ahmed N, Vogel B, Rohde E, Strunk D, Grifka J, Schulz MB and Grassel S: CD45-positive cells of haematopoietic origin enhance chondrogenic marker gene expression in rat marrow stromal cells. Int J Mol Med 18: 233-240, 2006.
24. Johnstone B, Hering TM, Caplan AI, Goldberg VM and Yoo JU: In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 238: 265-272, 1998.
25. Hauselmann HJ, Fernandes RJ, Mok SS, Schmid TM, Block JA, Aydelotte MB, Kuettner KE and Thonar EJ: Phenotypic stability of bovine articular chondrocytes after long-term culture in alginate beads. J Cell Sci 107: 17-27, 1994.
26. Ginzinger DG: Gene quantification using real-time quantitative PCR: an emerging technology hits the mainstream. Exp Hematol 30: 503-512, 2002.
27. Pfaffl MW: A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45, 2001.
28. Bustin SA, Benes V, Nolan T and Pfaffl MW: Quantitative real-time RT-PCR-a perspective. J Mol Endocrinol 34: 597-601, 2005.
29. Bianco P, Riminucci M, Gronthos S and Robey PG: Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 19: 180-192, 2001.
30. Jones EA, Kinsey SE, English A, Jones RA, Straszynski L, Meredith DM, Markham AF, Jack A, Emery P and McGonagle D: Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum 46: 3349-3360, 2002.
31. Jefferies WA, Brandon MR, Williams AF and Hunt SV: Analysis of lymphopoietic stem cells with a monoclonal antibody to the rat transferrin receptor. Immunology 54: 333-341, 1985.
32. Buravkova LB and Anokhina EB: Effect of hypoxia on stromal precursors from rat bone marrow at the early stage of culturing. Bull Exp Biol Med 143: 411-413, 2007.
33. Deschaseaux F, Gindraux F, Saadi R, Obert L, Chalmers D and Herve P: Direct selection of human bone marrow mesenchymal stem cells using an anti-CD49a antibody reveals their low phenotype. Br J Haematol 122: 506-517, 2003.
34. Gindraux F, Selmani Z, Obert L, Davani S, Tiberghien P, Herve P and Deschaseaux F: Human and rodent bone marrow mesenchymal stem cells that express primitive stem cell markers can be directly enriched by using the CD49a molecule. Cell Tissue Res 327: 471-483, 2007.
35. Woollett GR, Barclay AN, Puklavec M and Williams AF: Molecular and antigenic heterogeneity of the rat leukocyte-common antigen from thymocytes and T and B lymphocytes. Eur J Immunol 15: 168-173, 1985.
36. Javazon EH, Colter DC, Schwarz EJ and Prockop DJ: Rat marrow stromal cells are more sensitive to plating density and expand more rapidly from single-cell-derived colonies than human marrow stromal cells. Stem Cells 19: 219-225, 2001.
37. Camper L, Hellman U and Lundgren-Akerlund E: Isolation, cloning, and sequence analysis of the integrin subunit alpha10, a beta1-associated collagen binding integrin expressed on chondrocytes. J Biol Chem 273: 20383-20389, 1998.
38. Camper L, Holmvall K, Wangnerud C, Aszodi A and Lundgren-Akerlund E: Distribution of the collagen-binding integrin alpha10beta1 during mouse development. Cell Tissue Res 306: 107-116, 2001.
39. Mayer H, Bertram H, Lindenmaier W, Korff T, Weber H and Weich H: Vascular endothelial growth factor (VEGF-A) expression in human mesenchymal stem cells: autocrine and paracrine role on osteoblastic and endothelial differentiation. J Cell Biochem 95: 827-839, 2005.
40. Hoffmann A, Czichos S, Kaps C, Bachner D, Mayer H, Kurkalli BG, Zilberman Y, Turgeman G, Pelled G, Gross G and Gazit D: The T-box transcription factor Brachyury mediates cartilage development in mesenchymal stem cell line C3H10T1/2. J Cell Sci 115: 769-781, 2002.
41. Xu J, Wang W, Ludeman M, Cheng K, Hayami T, Lotz JC and Kapila S: Chondrogenic differentiation of human mesenchymal stem cells in three-dimensional alginate gels. Tissue Eng 14: 667-680, 2008.
42. Zhao Q, Eberspaecher H, Lefebvre V and de Crombrugghe B: Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis. Dev Dyn 209: 377-386, 1997.
43. Okubo Y and Reddi AH: Thyroxine downregulates Sox9 and promotes chondrocyte hypertrophy. Biochem Biophys Res Commun 306: 186-190, 2003.
44. Akiyama H, Chaboissier MC, Martin JF, Schedl A and de Crombrugghe B: The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev 16: 2813-2828, 2002.
45. De Crombrugghe B, Lefebvre V, Behringer RR, Bi W, Murakami S and Huang W: Transcriptional mechanisms of chondrocyte differentiation. Matrix Biol 19: 389-394, 2000.
46. Schmid TM, Popp RG and Linsenmayer TF: Hypertrophic cartilage matrix. Type X collagen, supramolecular assembly, and calcification. Ann NY Acad Sci 580: 64-73, 1990.
47. Zheng Q, Zhou G, Morello R, Chen Y, Garcia-Rojas X and Lee B: Type X collagen gene regulation by Runx2 contributes directly to its hypertrophic chondrocyte-specific expression in vivo. J Cell Biol 162: 833-842, 2003.
48. Mwale F, Stachura D, Roughley P and Antoniou J: Limitations of using aggrecan and type X collagen as markers of chondrogenesis in mesenchymal stem cell differentiation. J Orthop Res 24: 1791-1798, 2006.
49. Pelttari K, Steck E and Richter W: The use of mesenchymal stem cells for chondrogenesis. Injury 39: S58-S65, 2008.
50. Silva WA Jr, Covas DT, Panepucci RA, Proto-Siqueira R, Siufi JL, Zanette DL, Santos AR and Zago MA: The profile of gene expression of human marrow mesenchymal stem cells. Stem Cells 21: 661-669, 2003.
51. Mannello F, Tonti GA, Bagnara GP and Papa S: Role and function of matrix metalloproteinases in the differentiation and biological characterization of mesenchymal stem cells. Stem Cells 86: 475-481, 2005.
52. Cronwright G, Le Blanc K, Gotherstrom C, Darcy P, Ehnman M and Brodin B: Cancer/testis antigen expression in human mesenchymal stem cells: down-regulation of SSX impairs cell migration and matrix metalloproteinase 2 expression. Cancer Res 65: 2207-2215, 2005.
53. Tuckermann JP, Pittois K, Partridge NC, Merregaert J and Angel P: Collagenase-3 (MMP-13) and integral membrane protein 2a (Itm2a) are marker genes of chondrogenic/osteoblastic cells in bone formation: sequential temporal, and spatial expression of Itm2a, alkaline phosphatase, MMP-13, and osteocalcin in the mouse. J Bone Miner Res 15: 1257-1265, 2000.
54. Stetler-Stevenson WG and Seo DW: TIMP-2: an endogenous inhibitor of angiogenesis. Trends Mol Med 11: 97-103, 2005.
55. Kinnaird T, Stabile E, Burnett MS, Shou M, Lee CW, Barr S, Fuchs S and Epstein SE: Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 109: 1543-1549, 2004.
56. Liu CH and Hwang SM: Cytokine interactions in mesenchymal stem cells from cord blood. Cytokine 32: 270-279, 2005.
57. Pufe T, Harde V, Petersen W, Goldring MB, Tillmann B and Mentlein R: Vascular endothelial growth factor (VEGF) induces matrix metalloproteinase expression in immortalized chondrocytes. J Pathol 202: 367-374, 2004.
58. Rehman J, Li J, Orschell CM and March KL: Peripheral blood 'endothelial progenitor cells' are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 107: 1164-1169, 2003.
59. Iba O, Matsubara H, Nozawa Y, Fujiyama S, Amano K, Mori Y, Kojima H and Iwasaka T: Angiogenesis by implantation of peripheral blood mononuclear cells and platelets into ischemic limbs. Circulation 106: 2019-2025, 2002.
60. Nakagawa H, Komorita N, Shibata F, Ikesue A, Konishi K, Fujioka M and Kato H: Identification of cytokine-induced neutrophil chemoattractants (CINC), rat GRO/CINC-2 alpha and CINC-2 beta, produced by granulation tissue in culture: purification, complete amino acid sequences and characterization. Biochem J 301: 545-550, 1994.
61. Quirici N, Soligo D, Bossolasco P, Servida F, Lumini C and Deliliers GL: Isolation of bone marrow mesenchymal stem cells by anti-nerve growth factor receptor antibodies. Exp Hematol 30: 783-791, 2002.
62. Yaghoobi MM and Mowla SJ: Differential gene expression pattern of neurotrophins and their receptors during neuronal differentiation of rat bone marrow stromal cells. Neurosci Lett 397: 149-154, 2006.
63. Yada M, Yamaguchi K and Tsuji T: NGF stimulates differentiation of osteoblastic MC3T3-E1 cells. Biochem Biophys Res Commun 205: 1187-1193, 1994.
64. Mezquita P, Parghi SS, Brandvold KA and Ruddell A: Myc regulates VEGF production in B cells by stimulating initiation of VEGF mRNA translation. Oncogene 24: 889-901, 2005.
65. Sherer TB, Neff PS and Tuttle JB: Increased nerve growth factor mRNA stability may underlie elevated nerve growth factor secretion from hypertensive vascular smooth muscle cells. Brain Res Mol Brain Res 62: 167-174, 1998.
66. Sherer TB, Neff PS, Hankins GR and Tuttle JB: Mechanisms of increased NGF production in vascular smooth muscle of the spontaneously hypertensive rat. Exp Cell Res 241: 186-193, 1998.